The niche for spermatogonial stem cells in the mammalian testis

International Journal of Hematology

Volumn 82, Issue 5, 2005, Pages 381-388

  Ogawa, Takehiko ^a   Ohmura, Masako ^b   Ohbo, Kazuyuki ^b  

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KEIO UNIVERSITY   (Japan)

Author keywords

Germ cell; Niche; Spermatogonia; Stem cell; Transplantation

Indexed keywords

BUSULFAN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; PROTEIN RET;

BASEMENT MEMBRANE; CELL CULTURE; CELL DIFFERENTIATION; CELL RENEWAL; DROSOPHILA; EMBRYO DEVELOPMENT; GERM CELL; GERM LINE; HEMATOPOIETIC STEM CELL; MAMMAL; MICROENVIRONMENT; NONHUMAN; REVIEW; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL; STEM CELL TRANSPLANTATION; TESTIS; ANIMAL; CYTOLOGY; HUMAN; MALE; METABOLISM; MOUSE; MUCOSA; PHYSIOLOGY; TRANSPLANTATION;

ANIMALS; HUMANS; MALE; MICE; MUCOUS MEMBRANE; SEMINIFEROUS TUBULES; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS;

EID: 33646465566     PISSN: 09255710     EISSN: None     Source Type: Journal    
DOI: 10.1532/IJH97.05088     Document Type: Review

References (72)

1. Morrison SJ, Weissman IL. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity. 1994;1:661-673.
2. Lagasse E, Shizuru JA, Uchida N, Tsukamoto A, Weissman IL. Toward regenerative medicine. Immunity. 2001;14:425-436.
3. Tegelenbosch RA, De Rooij DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res. 1993;290:193-200.
4. Nagano MC. Homing efficiency and proliferation kinetics of male germ line stem cells following transplantation in mice. Biol Reprod. 2003;69:701-707.
5. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273:242-245.
6. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4:7-25.
7. Xie T, Spradling AC. A niche maintaining germ line stem cells in the Drosophila ovary. Science. 2000;290:328-330.
8. Tran J, Brenner TJ, DiNardo S. Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature. 2000; 407:754-757.
9. Kiger AA, White-Cooper H, Fuller MT. Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature. 2000;407:750-754.
10. Lin H. The stem-cell niche theory: lessons from flies. Nat Rev Genet. 2002;3:931-940.
11. Gilboa L, Lehmann R. How different is Venus from Mars? The genetics of germ-line stem cells in Drosophila females and males. Development. 2004;131:4895-4905.
12. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836-841.
13. Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841-846.
14. Shen Q, Goderie SK, Jin L, et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science. 2004;304:1338-1340.
15. Arai F, Hirao A, Ohmura M, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118:149-161.
16. Huckins C. The spermatogonial stem cell population in adult rats, I: their morphology, proliferation and maturation. Anat Rec. 1971; 169:533-558.
17. Oakberg EF. Spermatogonial stem-cell renewal in the mouse. Anat Rec. 1971;169:515-532.
18. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A. 1994;91:11298-11302.
19. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A. 1994;91:11302-11307.
20. Kanatsu-Shinohara M, Ogonuki N, Inoue K, et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod. 2003;69:612-616.
21. McLaren A. Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol. 2000;163:3-9.
22. McCarrey JR. Development of the germ cell. In: Desjardins C, Ewing LL, eds. Cell and Molecular Biology of the Testis. Oxford, UK: Oxford University Press; 1993:58-89.
23. De Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl. 2000;21:776-798.
24. Brawley C, Matunis E. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science. 2004;304:1331-1334.
25. Loeffler M, Potten CS. Stem cells and cellular pedigrees: a conceptual introduction. In: Potten CS, ed. Stem Cells. London, UK: Academic Press; 1997:1-27.
26. Huckins C. The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium. Anat Rec. 1978;190:905-926.
27. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y. Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl2 in spermatogonia. Development. 1996;122:1703-1709.
28. Rodriguiz I, Ody C, Araki K, Garcia I, Vassalli P. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J. 1997;16:2262-2270.
29. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science. 1995;270:96-99.
30. Russell LD. Morphological and functional evidence for Sertoli-germ cell relationships. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater, Fla: Cache River Press; 1993:365-390.
31. Chiarini-Garcia H, Hornick JR, Griswold MD, Russell LD. Distribution of type A spermatogonia in the mouse is not random. Biol Reprod. 2001;65:1179-1185.
32. Chiarini-Garcia H, Raymer AM, Russell LD. Non-random distribution of spermatogonia in rats: evidence of niches in the seminiferous tubules. Reproduction. 2003;126:669-680.
33. Brinster RL. Germline stem cell transplantation and transgenesis. Science. 2002;296:2174-2176.
34. Ogawa T. Spermatogonial transplantation: the principle and possible applications. J Mol Med. 2001;79:368-374.
35. Creemers LB, Meng X, den Ouden K, et al. Transplantation of germ cells from glial cell line-derived neurotrophic factor-overexpressing mice to host testes depleted of endogenous spermatogenesis by fractionated irradiation. Biol Reprod. 2002;66:1579-1584.
36. Ogawa T, Aréchaga JM, Avarbock MR, Brinster RL. Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol. 1997;41:111-122.
37. Nagano M, Avarbock MR, Brinster RL. Pattern and kinetics of donor mouse spermatogonial stem cell colonization in recipient testes. Biol Reprod. 1999;60:1429-1436.
38. Ross MH. Sertoli-Sertoli junctions and Sertoli-spermatid junctions after efferent ductule ligation and lanthanum treatment. Am J Anat. 1977;148:49-55.
39. Ogawa T, Ohmura M, Yumura Y, Sawada H, Kubota Y. Expansion of murine spermatogonial stem cells through serial transplantation. Biol Reprod. 2003;68:316-322.
40. Dobrinski I, Ogawa T, Avarbock MR, Brinster RL. Computer assisted image analysis to assess colonization of recipient seminiferous tubules by spermatogonial stem cells from transgenic donor mice. Mol Reprod Dev. 1999;53:142-148.
41. Russell LD, Brinster RL. Spermatogonial transplantation. In: Zirkin BR, ed. Germ Cell Development, Division, Disruption and Death. New York, NY: Springer-Verlag; 1998:19-27.
42. Matsuzaki Y, Kinjo K, Mulligan RC, Okano H. Unexpectedly efficient homing capacity of purified murine hematopoietic stem cells. Immunity. 2004;20:87-93.
43. Ogawa T, Dobrinski I, Brinster RL. Recipient preparation is critical for spermatogonial transplantation in the rat. Tissue Cell. 1999;31:461-472.
44. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. Proc Natl Acad Sci U S A. 2000;98:6186-6191.
45. Ryu B-Y, Orwig KE, Avarbock MR, Brinster RL. Stem cell and niche development in the postnatal rat testis. Dev Biol. 2003;263:253-263.
46. 6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci U S A. 1999;96:5504-5509.
47. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Natl Acad Sci U S A. 2000;97:8346-8351.
48. Kubota H, Avarbock MR, Brinster RL. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci U S A. 2003;100:6487-6492.
49. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183:1797-1806.
50. Goodell MA, Rosenzweig M, Kim H, et al. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med. 1997;3:1337-1345.
51. Gussoni E, Soneoka Y, Strickland CD, et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 1999;401:390-394.
52. pos cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol. 2002;245:42-56.
53. Murayama A, Matsuzaki Y, Kawaguchi A, Shimazaki T, Okano H. Flow cytometric analysis of neural stem cells in the developing and adult mouse brain. Neurosci Res. 2002;69:837-847.
54. Shimano K, Satake M, Okaya A, et al. Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1. Am J Pathol. 2003;163:3-9.
55. Lassalle B, Bastos H, Louis JP, et al. 'Side Population' cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells. Development. 2004;131:479-487.
56. Falciatori I, Borsellino G, Haliassos N, et al. Identification and enrichment of spermatogonial stem cells displaying side-population phenotype in immature mouse testis. FASEB J. 2004;18:376-378.
57. Siminovitch L, Till JE, McCulloch EA. Decline in colony forming ability of marrow cells subjected to serial transplantation into irradiated mice. J Cell Physiol. 1964;64:23-31.
58. Iscove NN, Nawa K. Hematopoietic stem cells expand during serial transplantation in vivo without apparent exhaustion. Curr Biol. 1997;7:805-808.
59. Kanatsu-Shinohara M, Toyokuni S, Morimoto T, et al. Functional assessment of self-renewal activity of male germline stem cells following cytotoxic damage and serial transplantation. Biol Reprod. 2003;68:1801-1807.
60. Kierszenbaum AL. Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. Endocr Rev. 1994;15:116-134.
61. Staub C. A century of research on mammalian male germ cell meiotic differentiation in vitro. J Androl. 2001;22:911-926.
62. Meng X, Lindahl M, Hyvonen ME, et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science. 2000;287:1489-1493.
63. Yomogida K, Yagura Y, Tadokoro Y, Nishimune Y. Dramatic expansion of germinal stem cells by ectopically expressed human glial cell line-derived neurotrophic factor in mouse Sertoli cells. Biol Reprod. 2003;69:1303-1307.
64. Tadokoro Y, Yomogida K, Ohta H, Tohda A, Nishimune Y. Homeostatic regulation of germinal stem cell proliferation by the GDNF/ FSH pathway. Mech Dev. 2002;113:29-39.
65. Matzuk MM. Germ-line immortality. Proc Natl Acad Sci U S A. 2004; 101:16395-16396.
66. Nagano M, Ryu BY, Brinster CJ, Avarbock MR, Brinster RL. Maintenance of mouse male germ line stem cells in vitro. Biol Reprod. 2003;68:2207-2214.
67. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A. 2004;101:16489-16494.
68. Ogawa T, Ohmura M, Tamura Y, et al. Derivation and morphological characterization of mouse spermatogonial stem cell lines. Arch Histol Cytol. 2004;67:297-306.
69. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell. 2004;116:769-778.
70. Ohmura M, Ogawa T, Ono M, et al. Increment of murine spermatogonial cell number by gonadotropin-releasing hormone analogue is independent of stem cell factor c-kit signal. Biol Reprod. 2003;68:2304-2313.
71. Kanatsu-Shinohara M, Miki H, Inoue K, et al. Long-term culture of mouse male germline stem cells under serum- or feeder-free conditions. Biol Reprod. 2005;72:985-991.
72. Clermont Y. Introduction to the Sertoli cell. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater, Fla: Cache River Press; 1993:xxi-xxv.